Contagious yawning-the urge to yawn when
thinking about, listening to, or viewing
yawning-is a well-documented phenomenon in
humans and animals. The reduced yawn contagion
observed in the autistic population suggested
that it might be empathy related; however, it is
unknown whether such a connection applies to
nonclinical populations. We examined influences
from both empathy (i.e., autistic traits) and
nonempathy factors (i.e., individuals'
perceptual detection sensitivity to yawning,
happy, and angry faces) on 41 nonclinical
adults. We induced contagious yawning with a
5-minute video and 20 yawning photo stimuli. In
addition, we measured participants' autistic
traits (with the autism-spectrum quotient
questionnaire), eye gaze patterns, and their
perceptual thresholds to detect yawning and
emotion in human face photos. We found two
factors associated with yawning contagion: (a)
those more sensitive to detect yawning, but not
other emotional expressions, displayed more
contagious yawning than those less sensitive to
yawning expressions, and (b) female participants
exhibited significantly more contagious yawning
than male participants. We did not find an
association between autistic trait and
contagious yawning. Our study offers a working
hypothesis for future studies, in that
perceptual encoding of yawning interacts with
susceptibility to contagious yawning.

Contagious yawning, the urge to yawn when
thinking about, listening to, or viewing yawning
(Baenninger, 1987), is a well-documented
phenomenon observed in human beings, primates
(Anderson, Myowa-Yamakoshi, & Matsuzawa,
2004), and dogs (Harr, Gilbert, & Phillips,
2009). Despite research e_orts across more than
three decades, the underlying mechanism of
contagious yawning remains unclear. However, an
expanding range of hypotheses have been
proposed, including an innate releasing
mechanism (Provine, 1986, 1989), respiratory or
circulatory, thermoregulation, the arousal
hypothesis, and the social communication view
(for a review, see Guggisberg, Mathis, Schnider,
& Hess, 2010). Among them, the most
intriguing hypothesis that has aroused many
researchers' interest is the link between
empathy and contagious yawning. For instance,
Platek, Critton, Myers, and Gallup (2003) found
that contagious yawning could be understood as a
social behavior that involves mental attribution
(i.e., the propensity to understand another's
mental state). They found that individuals with
higher susceptibility to contagious yawning are
better at recognizing their own faces (i.e.,
self- face recognition) and theory of mind tasks
that capture one's social understanding.

If contagious yawning is indeed a social
behavior, what is its purpose? Guggisberg and
coworkers (2010) attempted to explain the social
function of contagious yawning by proposing
yawning as a communication signal that spread to
other people for survival purposes (i.e., the
social or communication hypothesis of yawning).
While the biological foundation of yawning might
be a change in physiological state (e.g., lung
oxygen levels decrease or brain temperature
increases) in response to our environment, they
proposed that the contagious e_ect of yawning
allowed us to communicate with our social group
and promotes behavioral synchronization for
facing potential threat. Indeed, this idea is
not entirely novel&emdash;in an earlier study,
Provine (1989) stated that ''the chain reaction
of contagious yawning synchronizes the
physiological as well as behavioral state of the
group'' (p. 213). Similarly, Brothers (1990)
introduced the idea that yawning could be a form
of social signaling akin to laughter that is
contagious. Although speculative, the social or
communication hypothesis helps explain the
social function of contagious yawning and
suggests an account for the relationship between
contagious yawning and social
understanding.

Neuroimaging studies have found that brain
regions associated with contagious yawning are
also related to social understanding and
empathy. Activation in the ventromedial
prefrontal cortex, which is known for the
processing of social cues and recognition of
complex emotional expression (Eslinger &
Damasio, 1985; Wager, Phan, Liberzon, &
Taylor, 2003), increased during free viewing of
a yawning video but not when the video stimuli
displayed gaping, coughing, or expressionless
faces (Nahab, Hattori, Saad, & Hallet,
2009). Schu¨ rmann et al. (2005) showed
that BOLD response signals in the superior
temporal sulcus, a region known for being
involved in facial expression recognition and
empathy (see Narumoto, Okada, Sadato, Fukui,
& Yonekura, 2001; Calder & Young, 2005,
for a review), increased signiÞcantly when
participants watched yawning videos, but not
mouth opening videos, and was positively
associated with the urge to yawn. Platek,
Mohamed, and Gallup (2005) also revealed that
watching yawning videos evoked unique activation
in the posterior cingulate cortex and precuneus,
which play important roles in theory of mind and
social processing (Blakemore, Rees, & Frith,
1998; Fletcher et al., 1995). These studies
together suggest that brain regions involved in
social processing may be heavily involved in
contagious yawning.

Clinical reports also suggest that
individuals' social understanding may relate to
their susceptibility to contagious yawning.
Children aged 7 to 15 years who had been
diagnosed with an autism spectrum disorder
(ASD)&emdash;a range of developmental disorders
characterized by deÞcits in social
interaction&emdash;showed reduced contagious
yawning compared with typically developing (TD)
individuals when watching a yawning video but
not when watching a smiling video (Senju et al.,
2007). Helt, Eigsti, Snyder, and Fein (2010)
matched mental ages between ASD and TD children
aged 5 to 12 years and replicated the
Þnding that children with ASD were
signiÞcantly less likely than TD children
to yawn after being exposed to the
experimenter's yawn. In addition, Giganti and
Esposito Ziello (2009) compared the frequency of
contagious yawning between ASD children with
varied severity (characterized by the Childhood
Autism Rating Scale) and found that children
with low autistic severity elicited more
contagious yawning than those with high autistic
severity. The clinical reports signiÞed a
possible relationship between autistic
characteristics and susceptibility to contagious
yawning (Baron-Cohen, Leslie, & Frith, 1985;
Platek et al., 2003). Nonetheless, it is unclear
whether this connection applies to a nonautistic
population that can be viewed as a continuous
spectrum or exists only in the autistic
population.

Previous studies have indicated that even
among nonautistic populations, not all
individuals were susceptible to contagious
yawning. Only 40% to 60% of the nonautistic
population display contagious yawning in
response to a yawn stimulus (Hoogenhout, van der
Straaten, Pileggi, & Malcolm-Smith, 2013;
Platek et al., 2003), indicating individual
variability in susceptibility to contagious
yawning. However, little is known about factors
that determine such individual di_erences. To
our best knowledge, only one recent study
assessed a comprehensive range of factors in
explaining individual variation in
susceptibility to contagious yawning
(Bartholomew & Cirulli, 2014). Among all
variables (i.e., basic demographics, empathy,
sleep, cognitive performance, testing
conditions, and time of day), age, not empathy,
was the only factor that could
signiÞcantly predict individual variation
in susceptibility to contagious yawning: Older
participants yawned less than younger
participants. Yet, age only explained 8% of the
variation, which leaves a huge amount of
variation unexplained. Therefore, studies of
other variables beyond the commonly studied
social factors (e.g., empathy) are
warranted.

Apart from social di_culties, one well-known
characteristic of autistic people is their
atypical eye-gazing pattern during face
processing, that is, looking at the mouth more
than the eyes (Blair, 2005; Gepner, Gelder,
& Schonen, 1996; Golarai, Grill-Spector,
& Reiss, 2006). This perceptual distinction
was proposed as an alternative account for the
notable social deÞcits in the ASD
population: Their proclivity for not attending
to regions containing the most social
information (e.g., eyes) might create a
perceptual bottleneck for the subsequent
processing of social interactions (Baron-Cohen,
Wheelwright, & Jolli_e, 1997; Dawson et al.,
2004).

Interestingly, two recent Þndings
indicated that directing attention to the eyes
could e_ectively restore susceptibility to
contagious yawning in autistic individuals to
the same extent as nonautistic individuals.
Senju et al. (2009) instructed both participants
with and without autism to Þxate on a
location where the eyes of face stimuli would
appear. The participants were asked to count the
number of female faces while watching video
clips of yawning or control mouth movements.
When autistic individuals directed their
attention to the eyes, they displayed equally
frequent yawning responses toward yawning
stimuli as did nonautistic individuals. Yet,
this study lacked objective measurement (e.g.,
an eye tracker) of the actual eye gaze to
validate whether the e_ect was truly from gaze
redirection. With the assistance of an eye
tracker, Usui et al. (2013) initiated yawning or
control videos only after participating ASD
children had continuously Þxated on the
eye region of the actor for 500 ms. In the task,
participating children counted the number of
actors wearing glasses, and Usui et al. (2013)
replicated the results from Senju et al.'s
(2009) study. The importance of access to the
eye region of an inducing stimulus was reported
in nonclinical participants (Provine, 1989).
When participants viewed a variety of yawning
stimuli including a complete-face yawn, no-mouth
yawn, no-eyes yawn, and a control stimulus
(smile), complete-face yawns evoked
signiÞcantly more yawners than a control
smiling face (Provine, 1989). The ''no-mouth''
yawn was the only stimuli with deleted facial
features that generated as many yawners as the
complete-face yawn. Conceivably, removing facial
features of a yawn increases the detection
di_culty. This in turn diminishes the contagion
e_ect of yawning and evokes fewer yawners. This
Þnding also suggests that the eye region
may contain more fundamental information to
evoke contagious yawning than the mouth
region.

Other than experimental manipulation to
increase detection di_culty by reducing
accessibility of facial parts to viewers, does
an individual's inherent detection sensitivity
to a yawning expression preclude his or her
susceptibility to contagious yawning? This
question is currently unanswered. Similar to
contagious yawning, emotional contagion is well
documented as a highly unconscious and automatic
behavior of mimicking others' emotional
expression. Studies have shown that individuals
especially susceptible to emotional contagion
are those who can read others' emotional
expressions and are sensitive to others'
emotions (Doherty, 1997), and that those who
mimic others' expressions are better at
recognizing others' emotions (Oberman,
Winkielman, & Ramachandran, 2007; Stel &
van Knippenberg, 2008). Although yawning is not
considered an emotion and contagious yawning is
not understood as an example of emotional
contagion, it is possible that a similar
mechanism contributes to the individual
variation of both contagion phenomena.

The contagion e_ect occurs not only
unintentionally in higher level imitation such
as action or emotional contagion but also in
lower level nonemotional responses such as heart
rate (Dimascio, Boyd, & Greenblatt, 1957),
pupil size (del Valle Loarte & Garcia Ruiz,
2009; Harrison, Singer, Rotshtein, Dolan, &
Critchley, 2006), and temperature contagion
(Cooper et al., 2014). The temperature of a
participant's hand has been found to decrease
signiÞcantly after s/he observed and rated
the perceived temperature of actors whose hands
were immersed in ice-cold water. Since one
possible function of yawning is to lower our
body temperature to protect us from critical
brain temperature rises, it is possible that
both contagious yawning and temperature
contagion are important for temperature
regulation (Gallup & Eldakar, 2013; Gallup
& Gallup, 2008). Notably, the link between
sensitivity to temperature contagion and empathy
is not clear. A negative correlation between
sensitivity to temperature contagion and the
Mehrabian balanced emotional empathy scale (a
30-item questionnaire, including items such as
''It upsets me to see someone being mistreated''
rated on a 9-point agree-disagree scale that
assess individual's emotional empathy) was
found. However, a positive correlation was found
with the empathy concern subscale of the Davis
interpersonal reactivity scale rated on a
5-point scale (7-item Empathy Concern subscale
e.g., ''I often have tender, concerned feelings
for people less fortunate than me''). This
suggests that the relationship between
individual di_erences in empathy and low-level
contagion phenomena may not be a simple
one.

In this study, we contributed to the
little-investigated area of individual
di_erences in contagious yawning in a
nonclinical population by observing individuals'
autistic traits, and perceptual detection
sensitivity to yawning expressions. We aimed to
investigate the interplay between one's yawning
detection sensitivity and contagious yawning. We
Þrst attempted to extend the clinical
Þndings of the link between autistic
traits and contagious yawning to a nonclinical
sample by examining the association between
autism-spectrum quotient (AQ) scores and
contagious yawning. Then, we tested the
association between sensitivity to
emotional/yawning expressions and contagious
yawning. The study of individuals'
susceptibility to contagious yawning could
provide insight into psychiatric disorders such
as schizophrenia and autism, as well as general
human functioning related to yawning and the
contagion e_ect. Our hypotheses are as
follows:

2°) Individuals with higher sensitivity
to yawning expressions will display more
contagious yawning.

Discussion

This study revealed that an individual's
susceptibility to contagious yawning was
associated with his or her yawning detection
sensitivity. More speciÞcally, people with
higher perceptual detection sensitivity to
yawning are especially susceptible to contagious
yawning. We did not Þnd that autistic
tendencies in this nonclinical population were
associated with contagious yawning. We found an
unexpected gender e_ect: Females displayed more
contagious yawning than males. In summary,
gender and yawning detection sensitivity were
the two variables associated with individuals'
susceptibility for contagious yawning.

Our hypothesis that perceptual detection
sensitivity to yawning expression contributes to
the susceptibility of contagious yawning was
supported. Although the underlying mechanism
remained unclear, sensitivity to yawning could
be a possible precursor of contagious yawning
and might be facilitated by gazing at the eye
region of the inducer. This is in line with the
view from the perceptual perspective that
sensitivity to others' expressions (Provine,
1989) and proclivity to look at the eyes (Senju
et al., 2009; Usui et al., 2013) play a role in
determining the individual's susceptibility to
contagious yawning. These intriguing
Þndings directed the study of contagious
yawning from exploring a higher level of
processing (e.g., empathy) to a lower level of
processing (e.g., eye scanning patterns and
perceptual detection sensitivity). Our
Þndings add to the body of research
showing that perceptual detection sensitivity to
facial expression may alter one's social
processing. For example, Kuusikko et al. (2009)
used a computer-based emotional recognition test
and asked participants with autism to select the
correct upper facial basic emotion for each
picture. They found that autistic girls scored
lower in recognizing happiness and anger than
nonautistic girls. This implies a lower
sensitivity to emotional expressions and that
more cues may be required to detect an emotion.
This impedes their social processing and might
lead to inappropriate responses in social
interactions. Past studies found that patients
with depression also exhibit biased emotion
perception in emotional recognition tasks, in
which they demonstrated lower sensitivity than
controls when asked to distinguish happy from
neutral expression (Gur et al., 1992;
Mikhailova, Vladimirova, Iznak, Tsusulkovskaya,
& Sushko, 1996; Surguladze et al., 2004).
This reduced ability could have a
signiÞcant impact on a person's social
processing, which in turn could a_ect their own
emotion experiences. While earlier research on
contagious yawning highlighted its social and
empathetic components by showing that poorer
social understanding (e.g., in autism, Senju et
al., 2007; and schizophrenia, Platek et al.,
2003) depleted one's susceptibility to
contagious yawning, here we o_ered another
possible early perceptual origin. Hence, our
Þnding implied that the later processing
of the social information delivered by a yawn
may be precluded by low sensitivity to yawning
and results in a lower susceptibility to
contagious yawning.

In addition, our hypothesis that gaze to eye
regions enhanced one's perceptual detection
sensitivity to expressions including yawning was
partly supported by the positive association
between Þxation duration to the eye region
and perceptual detection sensitivity to yawning.
This Þnding is consistent with a study in
which eye-gazing patterns of autistic and
nonautistic children were recorded when they
viewed morphing facial expressions of six
di_erent emotions and labeled the emotions (Bal
et al., 2010). Results showed that looking more
at the eyes was associated with fewer errors in
recognition of disgust and surprise and faster
reaction times for recognizing fear but not
other emotions. This suggested that attention to
the eye region increased sensitivity to emotion
recognition, at least for fear, surprise, and
disgust. Our study extends this Þnding
beyond emotion recognition to the recognition of
yawning.

Our study also reported a female advantage
in susceptibility to contagious yawning, which
could originate from several possible sources.
First, a female advantage in yawning
susceptibility could come from a female bias in
empathetic ability (for a review, see Christov-
Moore et al., 2014), which is known to be
related to contagious yawning (Helt et al.,
2010; Nahab et al., 2009; Platek et al., 2005;
Schu¨ rmann et al., 2005; Senju et al.,
2007). Females score higher on self-reported
empathy questionnaires than males (Rueckert
& Naybar, 2008) and show stronger neural
activation in empathy-related brain regions such
as the amygdala (Schulte-Ru¨ ther,
Markowitsch, Shah, Fink, & Piefke, 2008).
However, in our sample, autistic tendency
measured by the AQ did not di_er between the two
genders. Second, females were reported to excel
in emotion recognition tasks (Hall &
Matsumoto, 2004; McClure, 2000; Montagne,
Kessels, Frigerio, de Haan, & Perrett, 2005;
Thompson & Voyer, 2014) and were
identiÞed as being better at expressing
their own emotions than men. Neuroimaging
studies also Þnd that females, but not
males, show increased activation of the right
inferior frontal cortex, which is known for
being involved in emotional contagion (Derntl et
al., 2010). In our sampled population, our
female participants had marginally
signiÞcant higher sensitivity than men in
detecting happy faces (p _ .063), but not in
angry or yawning faces. Therefore, there was no
direct evidence to connect this possibility to
our Þnding. Finally, females are more
sensitive to nonverbal cues in social
communication than men (Hall & Matsumoto,
2004; McClure, 2000; Montagne et al., 2005;
Thompson & Voyer, 2014). It is possible that
females are more susceptible to contagious
yawning than males due to their higher abilities
in understanding others' intention through
nonverbal cues like yawning. We have no direct
measurements to test this hypothesis, and this
will be a direction for future studies. Norscia
and coworkers (2016a) observed the natural
occurrence of contagious yawning among 92
nonstranger dyads and found that female
participants yawned more frequently than men in
response to others' yawning. As the
understanding of gender di_erence in the
contagion e_ect is still at its infancy, future
studies are warranted.

There are at least 15 negative reports on
gender di_erences in contagious yawning, and it
is worth noting the di_erences between them and
our study. First, 3 of the 15 studies
investigated children with autism (Helt et al.,
2010; Senju et al., 2007, 2009; Usui et al.,
2013), a population known to have a low yawning
frequency (Senju et al., 2007). This may limit
any detectable gender e_ect. Studies with
nonclinical populations (e.g., the current study
and Norscia et al., 2016a) might o_er a bigger
observable range. Moreover, a sexually immature
group like children is not a good sample group
for studying gender di_erences (Norscia, Demuru,
& Palagi, 2016b). Second, 5 of the 15
studies did not include a baseline condition to
control for spontaneous yawning (Bartholomew
& Cirulli, 2014; Eldakar et al., 2015;
Gallup, Church, Miller, Risko, & Kingstone,
2016; Gallup & Eldakar, 2011; Massen, Dusc,
Eldakar, & Gallup, 2014). A control
condition (i.e., in our case, a smiling video)
or a baseline measurement (e.g., spontaneous
yawning in Norscia et al., 2016a) o_ers an
assurance that the recorded yawning was not
predominantly spontaneous yawning, which is
known to have no gender di_erence (Schino &
Aureli, 1989), but contagious yawning which was
our central research interest. Lastly,
contagious yawning could be signiÞcantly
diminished by social presence (Gallup et al.,
2016), and females are more sensitive to social
etiquette (Baron-Cohen, O'Riordan, Jones, &
Plaisted, 1999). It is possible that the initial
female advantage to yawning susceptibility was
counterbalanced by the higher inhibition of
yawning behavior in females. Participants in 4
of the 15 studies were aware of experimenters'
observation of their yawning behavior as they
viewed the yawning photos directly in front of
the experimenter (Eldakar et al., 2015; Gallup
& Eldakar, 2011; Gallup & Gallup, 2007;
Massen et al., 2014). This makes it possible
that the gender di_erence was absent due to the
pressure to inhibit yawning behavior, especially
in females, due to the social presence of the
experimenters. To reduce participants' awareness
of having their yawning behavior observed, our
cover story disguised the real study purpose and
a hidden webcam was installed to record their
yawning for later analysis. In summary, our
control baseline, cover story, and experimental
design may o_er a more suitable combination to
observe a female advantage in susceptibility to
contagious yawning.

While a previous study reported that age is
the only variable contributing to individual
susceptibility to contagious yawning
(Bartholomew & Cirulli, 2014), we did not
Þnd similar evidence for older individuals
being less susceptible to yawning when they
watched yawning video clips and still images.
Our sample had a relatively narrow age range
(i.e., 19-26 years old) compared with
Bartholomew and Cirulli's study (i.e., 18-83
years old), hence, it may not be large enough to
reþect similar age e_ect.

Our Þnding that participants with more
autistic traits have a lower tendency to gaze at
eyes adds to recent reports of an association
between autistic traits and eye gazing in
nonclinical populations. Individuals with more
autistic traits (assessed using the Broad Autism
Phenotype Questionnaire) tended to look less at
the faces of experimenters who asked
participants questions (Vabalas & Freeth,
2016) and had shorter and less frequent saccades
on the face during a face-to-face interaction
with the experimenters (Freeth, Foulsham, &
Kingstone, 2013) compared with participants
lower in autistic traits. In a recognition task
of artiÞcial faces, Davis et al. (2017)
discovered that those who had higher AQ scores
on the AQ-social subscale tended to look less at
eye regions of the facial stimuli. Our results
extend the Þndings to human face photos
and videos and indicate that nonclinical
individuals lower in autistic traits tend to
gaze more at the eyes. This is supplementary to
the well-established report of individuals with
autism looking less at the eyes (Blair, 2005;
Gepner et al., 1996; Golarai et al., 2006).

However, we did not Þnd an association
between eye-gaze patterns and contagious
yawning. This is possibly because the face
studying patterns among the nonclinical
population were consistently concentrated on the
key features. The aforementioned studies
revealed the connection with contagious yawning
through comparisons between autistic and
nonautistic children (Senju et al., 2009; Usui
et al., 2013), which might cover a bigger range
of di_erences.

There are several possible directions for
future studies. Despite our e_orts in disguising
the main purpose of our study and minimizing
participants' awareness of their own yawning,
some participants still reported that they
suppressed their yawning due to social
etiquette. This could potentially a_ect
subjects' yawning frequency in response to the
yawning stimuli. We included a question on the
subjective urge to yawn as a supplementary tool
for measuring yawning tendency. In addition, a
more objective method, such as myography that
measures muscle activity, could be helpful to
measure subjects' yawning tendency, including
those that are suppressed and undetectable to
observation. Moreover, it is worth noting that
our yawning stimuli produced a þatter
psychometric curve than happy and angry stimuli.
All stimuli selected to construct psychometric
curves for the three expressions were based on
the same intensity rating method, so it is
unclear what constituted this di_erence. While
the faces considered as the happiest or angriest
in the rating task were always considered as
''YES-presence'' in the detection ask, and the
neutral faces are always considered as
''NO-presence'' in the detection ask, such
connection was less clear in yawning. One
possibility is that participants have adopted a
di_erent criterion in the Yes-No detection task
for yawning from that for happy or angry faces,
possibly due to the lack of experience on
yawning presence judgment. It is still an
unsolved puzzle to us why this occurs, and it
may be a possible direction for future study.
Lastly, a more extensive screening to exclude
participants with clinical conditions and
trait-like alexithymia (the lack of own emotion
understanding) could be applied in future
studies. Individuals with psychiatric disorders
such as autism and schizophrenia could have
lower susceptibility to contagious yawning, and
individuals with alexithymia (which could be
measured with the Toronto Alexithymia Scale,
Bagby, Parker, & Taylor, 1994; Bird, Press,
& Richardson, 2011) may be limited to report
accurately on their urge to yawn. Our
postexperiment questionnaire showed that our
participants were not diagnosed with any
psychiatric disorders, and it may be desirable
to employ a more extensive pretest screening to
rule out factors that could a_ect sensitivity
and susceptibility to yawning in future
studies.

Conclusion

Our study revealed that participants with
higher yawning sensitivity (but not emotional
sensitivity) are more susceptible to contagious
yawning, which adds to the growing literature
that suggests perceptual deÞcits, such as
atypical eye-gaze patterns, might contribute to
reduced behavioral contagion. In addition,
females were found to display more contagious
yawning than males, and the underlying mechanism
awaits elucidation by future studies. These
Þndings have important theoretical
implications for understanding the mechanism of
contagious yawning for a nonautistic population.
It will be interesting to see whether similar
associations exist in a clinical population such
as people with autism.

In conclusion, our study offers a working
hypothesis for future studies to investigate how
the perceptual encoding of yawning interacts
with susceptibility to contagious yawning.